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Addressing Foodborne Threats to Health: Policies, Practices, and Global Coordination - Workshop Summary 3 Investigating Foodborne Threats OVERVIEW Foodborne illness is estimated to affect more than 76 million people in the United States each year, resulting in 325,000 hospitalizations and 5,200 deaths, but its true incidence is unknown (Mead et al., 1999). Because foodborne disease is difficult to diagnose, the vast majority of these illnesses and more than half of such deaths are attributed to “unknown agents” (Mead et al., 1999). The annual cost of medical expenses and productivity losses associated with the five most prevalent, diagnosable foodborne illnesses is nearly $7 billion (Vogt, 2005). Many people with symptoms of foodborne illness do not seek medical attention, further contributing to underdiagnosis. These circumstances, in addition to the rapid distribution of food on both a national and global scale, make it nearly impossible to detect even a large foodborne outbreak in time to limit its impact; see, for example, the description of the 1994 Salmonella outbreak in ice cream, described by Osterholm in Chapter 1. Most often, outbreak investigations occur after the fact. However, as the papers in this chapter illustrate, findings from outbreak investigations enable public health authorities to identify new foodborne pathogens, trace their entry into the food chain, and thereby reveal opportunities to improve food safety. The first contribution to this chapter, by Robert Tauxe of the Centers for Disease Control and Prevention (CDC), provides an overview of the foodborne threat spectrum and the practices of public health surveillance by which these microbes, and the burden of disease they cause, have become known. Tauxe explores several recent advancements in this field, including the development of information networks for foodborne disease surveillance (see also Besser in Chapter 5)
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Addressing Foodborne Threats to Health: Policies, Practices, and Global Coordination - Workshop Summary and enhanced outbreak investigations, and their probable link to recent reductions in cases of several major foodborne diseases. Despite these improvements, the processes of outbreak detection and investigation remain highly challenging, as illustrated in the case studies that make up the remainder of this chapter. The first two papers, by Barbara Herwaldt of the CDC and Roberta Hammond and Dean Bodager of the Florida Department of Health, describe their experiences investigating a relatively new foodborne threat: the coccidian parasite Cyclospora cayetanensis. Little was known about the organism when, in the mid-1990s, large, multistate outbreaks of gastroenteritis were recognized. Herwaldt and public health colleagues eventually traced these outbreaks to raspberries from Guatemala, where Cyclospora infection is endemic. Several other types of fresh produce have also been identified as vehicles for cyclosporiasis outbreaks. Herwaldt analyzes the challenges presented by foodborne outbreaks (in general, as well as the specific difficulties associated with C. cayetanensis) and draws important lessons for the future of public health. In the subsequent paper, Hammond and Bodager describe the complexities of a recent C. cayetanensis investigation. Triggered by an early 2005 report from a private lab of an unusually large number of infections, the investigation ultimately involved county health departments throughout Florida, three different state agencies that regulate food in Florida, and two federal agencies: the CDC and the Food and Drug Administration (FDA). The investigators determined that imported basil provided the vehicle for the parasite; like raspberries, basil is a “stealth” ingredient that many people do not recognize or (because such foods are often served as garnishes) easily forget. Such accounts illustrate the importance of examining seemingly unrelated cases of apparent foodborne illnesses as indicators of outbreaks and pursuing them to their sources through timely and thorough investigation. The pathogen discussed in the chapter’s final contribution, the hepatitis A virus (HAV), is far better characterized than Cyclospora, yet its investigators are faced with a similar array of challenges. This paper, by workshop speaker Beth Bell and Anthony Fiore of the CDC, describes a series of hepatitis A outbreaks in late 2003 that included the largest such outbreak reported in the United States. It involved over 600 patrons of a single Pennsylvania restaurant, and ultimately led the FDA to ban imports from the Mexican farms that grew the tainted green onions that caused the outbreak. Investigators were aided by molecular methods for HAV detection (comparable methods do not exist for Cyclospora), but Bell and Fiore note several characteristics of routine hepatitis A surveillance and of the infection itself that continue to hinder its detection and control. The authors conclude that foodborne HAV infection (and those of other enteric pathogens) may be best prevented on the farm by reducing the contamination of produce with fecal material. Taken as a whole, the papers in this chapter demonstrate both the crucial importance and the daunting difficulty of conducting foodborne outbreak investi-
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Addressing Foodborne Threats to Health: Policies, Practices, and Global Coordination - Workshop Summary gations. The success of such investigations depends to a large extent on public and private laboratories that must have adequate resources if they are to quickly and accurately detect threats to our food supply. Indeed, Tauxe observes that future advancements in the detection and investigation of foodborne illness are less likely to be achieved through technical innovation than through the strengthening of public health infrastructure. THE BURDEN OF ILLNESS ASSOCIATED WITH FOODBORNE THREATS TO HEALTH, AND THE CHALLENGE OF PREVENTION Robert V. Tauxe, M.D., M.P.H.1 Centers for Disease Control and Prevention2 Few human endeavors are more complex than the constant, daily, and varied effort to produce and prepare the foods we eat. The many cultural traditions and changing tastes introduce new foods and food-making processes to growing populations around the world. As a result, the foodborne diseases that follow the contamination of the food supply with any of a large number of microbes and toxins present similarly evolving challenges. A new foodborne disease may emerge when a previously unknown pathogen appears in a reservoir related to the food supply or when transmission through a new foodborne pathway is documented for a known pathogen. When a new foodborne disease appears, there is a natural history to the challenge, starting with first detection and description; the development of means to diagnose and treat the new infection; investigations into the sources, reservoirs, and transmission pathways; and finally prevention stratagems that improve to the point that the disease no longer presents an important problem. Each of the many known foodborne diseases is somewhere on this progression, and more are likely to be appreciated in the future. The spectrum of foodborne diseases is a dynamic range of threats. An array of bacterial, viral, and parasitic pathogens that cause foodborne infections are currently recognized as public health problems in the United States. Among these, an important number have only been recognized as foodborne pathogens in the last three decades (Table 3-1). Some were first detected as pathogens in recent times and may represent the evolution of new combinations of virulence properties. For example, E. coli O157:H7, not detected at all before the 1970s and first recognized as a cause of human illness in 1982, became a major foodborne disease with a recognized bovine reservoir on several continents by the 1990s (Griffin and Tauxe, 1991). This pathogen evolved from precursors with 1 Captain, U.S. Public Health Service; Chief of Foodborne and Diarrheal Diseases Branch, Division of Bacterial and Mycotic Diseases, National Center for Infectious Diseases. 2 The findings and conclusions in this manuscript have not been formally disseminated by CDC and should not be construed to represent any agency determination or policy.
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Addressing Foodborne Threats to Health: Policies, Practices, and Global Coordination - Workshop Summary TABLE 3-1 Foodborne Pathogens in the United States Bacteria Viruses Bacillus cereus Norovirus* Brucella Rotavirus* Campylobacter* Astrovirus* Clostridium botulinum Hepatitis A Clostridium perfringens* Enterobacter sakazakii* Parasites E. coli O157:H7* Anisakis E. coli non-O157 STEC* Cryptosporidium* E. coli other diarrheogenic* Cyclospora* Mycobacterium bovis Giardia lamblia* Salmonella Typhi Toxoplasma* Salmonella nontyphoidal Trichinella Shigella Staphylococcus aureus Prions Streptococcus Bovine encephalopathy agent* Vibrio cholerae, toxigenic (O1 and O139)* Vibrio vulnificus* Vibrio parahaemolyticus* Yersinia enterocolitica* NOTE: Pathogens characterized as foodborne within the last 30 years are indicated with an asterisk. SOURCE: Tauxe (2005); Adapted from Tauxe (2002). far less pathogenic potential as the result of several phage-induced mutations (Wick et al., 2005). Though the timing of these modifications remains unproven, several have noted that mobilization of phages and of other transferable genetic elements could be linked to exposure to antimicrobial agents (Zhang et al., 2000; LeFebvre et al., 2005) and therefore perhaps linked to relatively recent changes in agriculture. Another recent example is the emergence of an entirely new toxigenic serotype of Vibrio cholerae with epidemic potential. This serotype, O139, first appeared in 1992 in India, and spread rapidly through much of South and Southeast Asia where it was transmitted through water and food (Hoge et al., 1996). This serotype appears to have evolved as the result of a horizontal transfer of the genes that produce the O-antigen, possibly from another Vibrio, into several strains of the dominant strain of epidemic toxigenic V. cholerae O1 (Faruque et al., 2003). Other pathogens were recognized as human pathogens well before they were linked to foodborne transmission. For example, Listeria monocytogenes, first described as a cause of severe invasive infections in humans in the 1930s, was first linked to foodborne transmission in 1981 in an outbreak associated with cole slaw (Schlech et al., 1983), and more recently it was documented to be primarily foodborne (Slutsker et al., 2000). Campylobacter jejuni, described as a cause of invasive infection in immunocompromised hosts in the 1950s, was shown in 1977
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Addressing Foodborne Threats to Health: Policies, Practices, and Global Coordination - Workshop Summary to be a common enteric pathogen in normal hosts; the importance of foodborne transmission was established by 1980 (Blaser et al., 1983). The more recent observations of the parasite Cyclospora cayetanensis show how a pathogen that was geographically restricted to remote and third-world locations may leap to the forefront as a new food safety challenge, as summarized elsewhere in this report. This means that the new and emerging foodborne pathogens observed elsewhere in the world are of substantial interest and may offer a view into our future. The recent reports of outbreaks of Yersinia pseudotuberculosis associated with lettuce in Finland and of hepatitis E infection associated with swine in Japan are worthy of our attention (Nuorti et al., 2004; Yazaki et al., 2003). Still others represent the recrudescence of foodborne challenges long brought under control, as changing tastes and patterns of trade reintroduce pathogens to the public that we last saw as a significant problem many decades ago. Souvenir seafood brought back in suitcases led to foodborne cholera in New Jersey in the 1990s (Finelli et al., 1992). The recent appearance of bovine tuberculosis in New York City may be a result of the rapid shipment of homemade cheeses from Latin America, made traditionally with unpasteurized milk (CDC, 2005a). The specter of an intentional attack on the population through the food supply has added other pathogens—new and old—to the list of potential threats (Sobel et al., 2002). We can anticipate new challenges to continue to emerge. A robust and flexible public health surveillance system is an important part of how we will detect, characterize, and ultimately prevent these new challenges. Public Health Surveillance Public health surveillance is conducted to define the magnitude and burden of a disease that needs public health action, to identify and investigate outbreaks so that control measures can be rapidly implemented and issues in need of further research swiftly identified, and to measure the impact of control and prevention efforts. The public health surveillance of infections that are likely to be foodborne now includes a substantial list of pathogens whose diagnosis is to be reported to public health authorities, and a new set of national networks for characterizing the pathogens and the illnesses they cause. The recent improvements in surveillance have been summarized in detail in a recent Institute of Medicine (IOM) publication (IOM/NRC, 2003). The following is a brief sketch of some of the improvements. The primary authority for surveillance rests with the state health departments, which gather information from cities and counties and operate most of the public health laboratories. State and local notifiable diseases laws request or require clinicians and laboratories to report specific infections and to refer isolates of some pathogens to the public health laboratory for further characterization. These laws also typically require the reporting of unusual clusters or outbreaks of disease. In addition, many jurisdictions maintain complaint lines, to which concerned
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Addressing Foodborne Threats to Health: Policies, Practices, and Global Coordination - Workshop Summary citizens may directly report illnesses or observations they think may need public health attention. Some food testing occurs in the course of routine inspections and as part of process monitoring within food production. This testing may also provide some information about the status of the food supply, though its purpose is usually the ongoing verification of process control, not safety testing of each lot. Since 1996, the public health surveillance system for foodborne diseases has been strengthened in several ways. Several diseases were added to the standard notifiable disease reporting system, including non-O157 Shiga toxin-producing E. coli, hemolytic uremic syndrome, Cyclospora cayetanensis, and Listeria monocytogenes. The routine public health serotyping of Salmonella and Shigella was strengthened by the production and distribution of new antisera and training in their use; now new DNA sequence-based methods are being developed for more rapid identification of the serotype of Salmonella (McQuiston et al., 2004). Public health monitoring of antimicrobial resistance in several enteric bacterial pathogens has been implemented in parallel with monitoring of resistance in the same pathogens isolated from animals and foods, leading to the identification of such hazards as fluoroquinolone-resistant Campylobacter jejuni and multi-drug resistant strains of Salmonella enteriticas serotype Typhimurium and Salmonella enteriticas serotype Newport (Holmes and Chiller, 2004). The reporting of outbreaks of foodborne diseases from local and state health departments has been improved by standardized and rapid reporting via the Internet and the Electronic Foodborne Outbreak Reporting System (CDC, 2005d). Enhanced surveillance, including a new collection form and improved close-out procedures doubled the number of foodborne outbreaks reported to more than 1,200 outbreaks each year (Figure 3-1). Now the Electronic Foodborne Outbreak Reporting System has changed an old and slow paper-based system into a more rapid reporting that makes it likely that a cluster of similar outbreaks occurring in several parts of the country at once will be detected and flagged, and also increasing the utility of the surveillance data to track trends in specific foodborne outbreak categories. PulseNet, CDC’s national network for subtyping foodborne bacterial pathogens, has been implemented in all 50 states and a growing number of large city health departments, as well as in the laboratories of the food regulatory agencies at the U.S. Department of Agriculture (USDA) and the FDA (Gerner-Smidt et al., 2006). This network relies on the submission of isolates of E. coli O157:H7, Listeria monocytogenes, Salmonella, and other bacterial pathogens from clinical laboratories to the public health laboratory, where the DNA “fingerprint” is determined using pulsed-field gel electrophoresis. Automated comparison of the digitized DNA pattern with the growing state and national database can swiftly identify strains (and therefore cases) that might be related, detecting clusters spread across multistate jurisdictions that might otherwise have been missed completely. In the 1960s, Salmonella serotyping transformed surveillance for that organism by increasing the signal-to-noise ratio and making it possible to pick
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Addressing Foodborne Threats to Health: Policies, Practices, and Global Coordination - Workshop Summary FIGURE 3-1 Reported outbreaks of foodborne diseases, 1990–2004, United States. SOURCE: Adapted from CDC (2006b). out outbreaks of one serotype from the background noise of all salmonellosis (CDC, 1965). Now PulseNet provides an additional specificity, with a generally applicable tool for identifying clusters of infections that are likely to be related, even within a single closely-related serotype such as E. coli O157:H7, or within individual Salmonella serotypes. PulseNet test protocols have now been developed for seven bacterial foodborne pathogens, as well as for Yersinia pestis and F. tularensis. PulseNet protocols have now been adopted in Canada, Japan, Australia and other countries and are the heart of international networks for surveillance in Europe, Asia and the Pacific, and Latin America (Swaminathan et al., 2006). This will enhance our own prevention capacity. For example, in 2004, public health laboratories in Japan detected a small cluster of E. coli O157:H7 infections in Okinawa that they linked to consuming ground beef from the commissary at a U.S. military base there, and an indistinguishable E. coli was detected in ground beef in Japan, which came from the United States (CDC, 2005b). The notification by Japan led to recall of 90,000 pounds of ground beef shipped to the military and other institutions in the United States. The same strain was also identified in two persons in the United States who did eat beef the origin of which was not traceable, and who would not otherwise have been linked. In the future, routine usage of multilocus variable number tandem repeat assays or other sequence based-methods in state health department laboratories will further refine the speed and precision of the network. However, the promise
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Addressing Foodborne Threats to Health: Policies, Practices, and Global Coordination - Workshop Summary of real-time results is more dependent on resources, rather than technology, including the vital participation of the private clinical laboratory sector to refer strains rapidly to the public health laboratory and on the laboratory support within the state health department to run the tests swiftly. Another major advance in foodborne surveillance has been FoodNet, the active sentinel site surveillance system for foodborne illness (Allos et al., 2004). While PulseNet enhances the ability of all states to detect clusters and investigate outbreaks, FoodNet is focused on developing standard and detailed surveillance data on sporadic (nonoutbreak-associated cases) in 10 sites around the country, now representing 14 percent of the U.S. population. Though sporadic cases are far more common than those that are associated with outbreaks, they receive far less attention in general. Active surveillance means that the health department regularly contacts the clinical laboratories to collect reports of what has been diagnosed, rather than relying on the laboratories to report them. In addition FoodNet conducts specialized surveys of the clinical laboratories, of the general population, and of other groups to obtain measures of the frequency of gastroenteritis in general, of specific diagnostic tests, and other measures important to interpreting surveillance data. Data from FoodNet have been critical to refining the overall estimates of the burden of foodborne disease and to tracking trends in specific infections over time. For example, between 1996 and 2004, FoodNet documented a 42 percent decline in diagnosed E. coli O157 infections, decreasing to 0.9 per 100,000 in the year 2004; a 40 percent decline in Listeria infections; and a 31 percent decline in Campylobacter infections (CDC, 2005c). With case-control and other studies, FoodNet also defines the association between infections and specific foods, contributing to the attribution of the burden of specific infections to foods. Increasingly, FoodNet serves as a platform for developing and evaluating improved public health surveillance and investigative and prevention strategies. Estimating the Burden of Foodborne Diseases The health burden of an infection includes the morbidity it causes, the hospitalization and other medical care that results, and the mortality, among other measures. Estimating this burden for a given pathogen means going beyond the reported cases. To contribute a reported case, the person must become ill, must seek medical care, the physician must ask for a laboratory test, the patient must provide a specimen for diagnostic study, the specimen must yield evidence of the pathogen, and the case must be reported. Slippage at each point means that the diagnosed cases are likely to represent only a small fraction of the cases that actually occur. Other measures of severe infection, such as hospital discharge summary records and cause of death as reported on death certificates, may be used to estimate the total number of hospitalizations and deaths due to acute enteric disease, but these measures significantly underreport specific infections,
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Addressing Foodborne Threats to Health: Policies, Practices, and Global Coordination - Workshop Summary as laboratory diagnoses may often not be reflected in the discharge or death certificate coding. In 1999, we published a report estimating the actual acute health burden of foodborne disease in the United States (Mead et al., 1999). These estimates were assembled from a variety of data collected by FoodNet and other sources. FoodNet population surveys measure the number of cases of acute gastroenteritis that actually occur and the proportion of these that seek care and are cultured (Herikstad et al., 2002). The FoodNet clinical laboratory surveys measure the likelihood that a specimen will be routinely tested for say, Salmonella or Campylobacter or E. coli O157 (Voetsch et al., 2004a). This information can then be used to amplify the number of cases that are diagnosed and reported; in this way FoodNet estimated that there are actually 38 cases of salmonellosis for every one that is diagnosed and reported (Voetsch et al., 2004b). FoodNet data also provide the number of diagnosed salmonellosis cases that lead to hospitalization and the number that lead to death. Doubling that number to account for cases that were not cultured provides a conservative estimate of the total number of hospitalizations and deaths. Using similar data and assumptions, the incidence of other infections under surveillance by FoodNet can also be estimated, and by use of a uniform set of assumptions and expert opinion it is possible to estimate the overall burden of known enteric infections at some 39 million infections per year (Mead et al., 1999). The next step was to estimate the proportion of these infections that are transmitted through food, rather than through water, direct contact with ill children, or other pathways. The estimated proportion of infections that are transmitted through foods varied by pathogen, and in sum was 38 percent. Thus, of 39 million enteric infections estimated to be caused by the known enteric pathogens, 16 million were attributed to food. A curious observation is that the estimate of acute enteric illness developed pathogen by pathogen (annual incidence of 39 million cases) is substantially less than the total amount of acute gastroenteritis in the population estimated by population survey (annual incidence of 211 million cases) (Mead et al., 1999). This “diagnostic gap” suggests that there are more pathogens yet to be discovered (Tauxe, 2002). The fraction of these other cases not accounted for by known pathogens that might be attributed to food is not directly measurable. The authors of the 1999 estimate chose 38 percent, the summary statistic for the known pathogens, as the best point estimate of what it might be for the other acute illnesses not accounted for by known pathogens. The final estimate, 76 million illnesses, 323,000 hospitalizations, and 5,000 deaths, refers to the year 1997. This comprehensive estimate is now being revised in a similar stepwise approach, starting with the measurement of the overall burden of acute gastroenteritis and with more refined and pathogen-specific approaches to the estimates of unreported illness. There are other ways of measuring the burden of unreported illness. In the United Kingdom, the Intestinal Infectious Diseases study empanelled a group of citizens who recorded their symptoms prospectively and provided stool speci-
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Addressing Foodborne Threats to Health: Policies, Practices, and Global Coordination - Workshop Summary mens for even mild cases of diarrheal illness (Wheeler et al., 1999). The Dutch SENSOR study followed a similar strategy, working with a group of sentinel general practitioners and their patients (de Wit et al., 2001). Both European approaches depended on the national healthcare system itself to provide a population-based framework, and both were sufficiently expensive that they have not been repeated. There are also measures of burden other than simple counts of cases, hospitalizations, and deaths. For example, the health-related costs for the principal bacterial foodborne pathogens (Salmonella, Campylobacter, E. coli O157, other Shiga-toxin-producing E. coli, and Listeria monocytogenes) have been estimated to be $6.9 billion (ERS, 2000). The cost to society associated with the estimated number of deaths that were not attributed to known etiologies could be as high as $17 billion, underlining the need for further refinement of this sector of the estimate (Frenzen, 2004). Inclusion of the postinfectious sequelae in the estimate can also greatly increase the economic burden. A detailed model developed for Campylobacter in the Netherlands included the burden of postinfectious arthritides and Guillain-Barre syndrome and measured the burden in disability-adjusted life years; this estimate indicated that a greater burden was due to the sequelae, rather than the acute illness (Havelaar et al., 2005). The industry costs of disrupted trade and development that can be occasioned by foodborne illness can be enormous, though they usually do not appear on the public health ledger. The costs of antimicrobial resistance associated with foodborne exposures have also not been estimated, but they might include the cost of illness caused by resistant foodborne pathogens and the costs related to the spread of transmissible resistance genes that are present in commensal organisms in the food supply, from which they may transfer to human pathogens. Prevention of Emerging Foodborne Threats: The Importance of the Outbreak Investigation The prevention of foodborne diseases in general is a complex effort, involving many different actors along the chain of production from the farm to food service. There are many different pathogens involved, almost none of which are vaccine preventable in the final consumer. Educating consumers, food handlers, and producers about their role in preventing foodborne disease is important, but not sufficient. Contamination of food can occur at many points from farm to table. Often the key to prevention is to understand those mechanisms of contamination well enough to prevent them, before the food reaches the final consumer. Investigation of contamination events, and especially investigation of outbreaks, is critical to understanding the mechanisms of contamination. Prevention often means reengineering food processes and policies for safety, usually with a focus on a specific food and/or pathogen. The foodborne outbreak investigation is thus a major driver for enhancing overall food safety. When an outbreak is detected, the first priority is to learn
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Addressing Foodborne Threats to Health: Policies, Practices, and Global Coordination - Workshop Summary enough to prevent further cases from occurring in the current outbreak. However, it is also an opportunity to learn something new, and to open research agendas with impact far beyond the one outbreak. Many foodborne pathogens were first identified in the course of an outbreak investigation. A new combination of pathogen and food may be revealed that needs further study by food scientists, animal and plant pathologists, as well as medical researchers. Just as the National Transportation Safety Board investigates a plane crash thoroughly after the fact to learn how to prevent similar ones, careful investigation even after an outbreak is over can define gaps in the system, stimulate further specific research, and indicate the needs for new processes or regulations. New combinations of specific pathogens and foods identified by outbreak investigations have been critical to guiding research and prevention (see Table 3-2). As the surveillance systems that we use in the United States have been enhanced in the last 10 years, we have observed a change in the number and nature of outbreaks detected. This is a paradox of surveillance: making surveillance better often reveals more of the problem, so that the actual public health burden appears worse. For example, as noted above, the number of foodborne outbreaks reported through the Electronic Foodborne Outbreak Reporting System doubled following relatively simple improvements in process and participation. PulseNet has caused a more substantial change in the nature of the outbreaks detected. By increasing the signal-to-noise ratio for specific pathogen subtypes, PulseNet makes it far more likely that geographically diffuse outbreaks will be detected. Those diffuse outbreaks are particularly instructive. PulseNet has had a profound impact on the kind of outbreaks that have been detected because the nature of the outbreaks detected depends critically on the methods used to detect them. If outbreaks only come to the attention of public health when concerned citizens, physicians, or healthcare facilities report them, then only large and locally apparent outbreaks are likely to be detected. These TABLE 3-2 Some New Pathogen-Food Combinations Characterized During Outbreak Investigations in the United States Pathogen Food E. coli O157 Beef, apple cider, and sprouts Salmonella serotype Enteritidis Eggs, broilers, and almonds Salmonella Poona Cantaloupe Multidrug resistant Salmonella Newport Ground beef and raw milk cheese Salmonella Javiana, Newport, and Braenderup Tomatoes Listeria monocytogenes Sliced luncheon turkey, hot dogs, and Mexican queso fresco Cyclospora Raspberries and basil Norovirus Raw oysters, salads, and sliced luncheon meats Hepatitis A Strawberries and green onions
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Addressing Foodborne Threats to Health: Policies, Practices, and Global Coordination - Workshop Summary tamination accounting for these earlier outbreaks. The outbreak strain from cases associated with the Pennsylvania outbreak (sequence D, Figure 3-9) turned out to be distinct from but closely related to the other outbreak strains, and fell into the same cluster of Mexico-related strains. These findings established that the four geographically separate but temporally related outbreaks represented at least three distinct events. Other States Not all hepatitis A is foodborne, and a common question that arises in the context of many foodborne hepatitis A outbreaks is the extent to which available surveillance methods are sensitive enough such that outbreak-associated cases or small clusters can be distinguished from “background” cases. This is particularly relevant for outbreaks, such as those described here, that are associated with a distributed food item, but in which the majority of cases are associated with exposure at a restaurant. Another “first” accomplished in the context of these investigations was an improvement in the sensitivity of surveillance by incorporating molecular methods. Comparison of strains identified during the outbreak period provided evidence that some apparently “sporadic” hepatitis A cases were indeed foodborne. Specimens were requested from any cases that did not have an identified source of transmission. Of over 50 specimens submitted, a number were identical to outbreak strains (Table 3-9) (Amon et al., 2005). TABLE 3-9 Source and Distribution of Cluster X Hepatitis A Virus Sequences, September–December 2003 (Outbreak Surveillance Specimens) and January 2002–August 2003 (Sentinel Counties and Mexico [BIDS*] specimens); n = 478 Cluster X non-A, B, D (n = 73) Sequence A (n = 54) Sequence B (n = 154) Sequence D (n = 197) Outbreak surveillance TN – 32 – – PA/OH/WV – – – 170 NC – – 10 – GA – 1 122 – Other 8 1 21 4 U.S. Sentinel Counties 23 – – 8 Mexico (BIDS)* 42 20 1 15 NOTE: TN, Tennessee; PA, Pennsylvania; OH, Ohio; WV, West Virginia; NC, North Carolina; GA, Georgia. *BIDS—Border Infectious Diseases Surveillance System. SOURCE: Amon et al. (2005).
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Addressing Foodborne Threats to Health: Policies, Practices, and Global Coordination - Workshop Summary Investigation of Farms Findings of molecular surveillance were consistent with sources in Mexico, as sequences matching each of the outbreak strains were identified from among BIDS specimens (Table 3-9). Four farms, all located in northern Mexico, potentially supplied the implicated restaurants, but no single farm could explain all four outbreaks. These traceback results were consistent with the results of sequencing—three distinct strains were identified from outbreak-associated cases in the four states. Representatives from the FDA and CDC visited the farms in question (FDA, 2003b). The harvesting procedure included a lot of handling of the onions, which were pulled from the ground by hand, after which the outer layer was peeled off, the roots were removed, the onions were cut to a consistent size, and they were banded into bunches. Packing involved spraying bunches with chlorinated water as they passed on a conveyor belt, followed by loading into a cardboard box which was topped with chipped ice. In the distribution network, boxes generally were not handled between the farm and the restaurant destination. A number of conditions on the farm were identified as areas of concern, including poor sanitation, inadequate hand washing facilities, worker health and hygiene, the quality of the water used in the fields at packing sheds, and the ice-making process. However, no single practice or event was identified that could have explained the outbreaks. Because HAV has no animal host, the original source of green onion contamination was a human infected with HAV and excreting the virus in stool. This fecal contamination could occur in a number of ways. Adults with contaminated hands could have touched the green onions during harvest or processing. Hepatitis A is endemic in Mexico, which means that the vast majority of the population is infected during childhood, and most adults are immune (Tanaka, 2000). Hence the majority of infections at any given time are occurring among children. Thus likely sources of contamination of hands include sewage or feces from workers’ HAV-infected children. It is also possible that HAV-infected children were present in the fields and contaminated the green onions directly. Direct contamination of the growing areas by sewage is also possible. Discussion The outbreaks described here were investigated rapidly and tracebacks were initiated early. However, a number of features of hepatitis A make detection and control of foodborne hepatitis A difficult, and the results of these investigations illustrate important areas of progress and remaining challenges (Fiore, 2004). Because HAV contamination of foods can be focal and the virus remains viable in the environment for months, cases can be both geographically and temporally dispersed. These investigations demonstrate the benefits of wider and faster use
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Addressing Foodborne Threats to Health: Policies, Practices, and Global Coordination - Workshop Summary of molecular epidemiologic methods, both in outbreak investigations and in the context of routine hepatitis A surveillance. Viral sequencing showed that four geographically separate outbreaks that occurred in the fall of 2003 represented at least three distinct events. Sequencing activities also improved the sensitivity of surveillance to define the scope of the outbreaks, distinguish outbreak-related from nonoutbreak-related cases, and identify evidence of sporadic unrecognized foodborne transmission. Finally, viral sequencing supported the results of the first traceback investigations and accelerated control efforts related to the outbreak in Pennsylvania. The investigations also exemplify challenges in foodborne hepatitis A outbreak response that stem from characteristics of routine hepatitis A surveillance and inherent aspects of the infection itself. Because cases reported through routine surveillance are not typically asked about foodborne exposures, the recognition of an unusual increase in the number of cases or of cases occurring among those in an unusual demographic group serves to alert authorities to begin asking about foodborne exposures as one potential common link among cases. However, even with the most rapid response and investigation of clusters of cases, the long incubation period of hepatitis A and inevitable delays in diagnosis and reporting necessitate a considerable lag time between exposure and the earliest possible detection of a foodborne outbreak. For example, the exposure that resulted in the outbreak in Pennsylvania was occurring as cases associated with the previous outbreaks were just being reported in the other states. Thus, even if a farm implicated in the earlier outbreaks had been linked to a farm implicated in the Pennsylvania outbreak, it is unlikely that even the most rapid of responses to the earlier outbreaks could have averted the subsequent outbreak in Pennsylvania. Green onions are emerging as a potential “problem” food, having been implicated in at least two previous restaurant-associated hepatitis A outbreaks (Dentinger et al., 2001; Datta et al., 2001). The vast majority of green onions consumed in the United States are imported from Mexico, a country in which hepatitis A is endemic (Calvin et al., 2004). They require extensive handling during harvest and may be particularly difficult to clean. A pattern of focal, low-level contamination in which possibly very few bunches were contaminated, may make it difficult to detect transmission when it occurs. The outbreak in Pennsylvania illustrates how conditions at the point of sale can amplify an outbreak. A combination of factors probably contributed to this outbreak’s size and high attack rate. The large number of diners who ate at the restaurant during the days of peak exposure were all offered mild salsa, the food item most strongly associated with illness. Preparation practices, such as rinsing green onions while they are still bundled and chopping and storage methods that allowed for cross-contamination, could also have contributed to the size of the outbreak. Because of the high concentration of HAV in stool and the likely low infectious dose, even a small amount of fecal contamination might result in many hundreds of infectious doses. Although the 2005 Food Code includes a require-
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Addressing Foodborne Threats to Health: Policies, Practices, and Global Coordination - Workshop Summary ment that vegetables that are not subsequently cooked be washed, it does not offer guidance about specific methods to prevent cross-contamination of produce (HHS, 2005). Progress has been made in developing methods to detect HAV in food, including reproducible methods to detect the virus in “spiked” food samples and produce washes (Shan et al., 2005). Although theoretically attractive, there are a number of difficulties inherent in attempting to detect HAV in produce. The virus does not multiply in foods, and the concentration may be quite low. However, viral culture is not feasible, so there is a need to rely on RT-PCR techniques, which may not perform consistently in the presence of complex food mixtures. Further, RT-PCR cannot distinguish infectious HAV from noninfectious HAV RNA. Even if these technical problems were solved, HAV detection in food is unlikely to be of much practical use in the context of outbreak investigations for a number of reasons. Perhaps most important, particularly in the case of produce, is that the implicated item has almost invariably been consumed or discarded by the time illness is occurring. Further, methods are not at a level of development as of yet such that they can be scaled up to volumes needed to be reasonably sure that contamination is not present, particularly given the low infectious dose. Finally, these currently available methods take days to complete. Perhaps most important is prevention of HAV (and other enteric pathogens) contamination of produce in the first place by preventing fecal contamination of produce on the farm. Hepatitis A is endemic in Mexico, and while the precise mechanism of transmission in the outbreaks described here could not be determined, control measures can be implemented that could prevent such outbreaks. These include ensuring that field workers are healthy and have access to adequate sanitary facilities and ensuring that water used to irrigate and rinse produce is not contaminated with feces. Children are the source of most transmission of HAV in rural communities in Mexico and much of the developing world, and children should not be present in areas where food is harvested. Reduction in HAV transmission among children in areas where produce is grown would further reduce opportunities for contamination. REFERENCES Alfano-Sobsey EM, Eberhard ML, Seed JR, Weber DJ, Won KY, Nace EK, Moe CL. 2004. Human challenge pilot study with Cyclospora cayetanensis. Emerging Infectious Diseases 10(4): 726–728. Allos B, Moore M, Griffin P, Tauxe R. 2004. Surveillance for sporadic foodborne disease in the 21st century: The FoodNet perspective. Clinical Infectious Diseases 38(Suppl 3):S115–S120. Amon JJ, Devasia R, Xia G, Nainan OV, Hall S, Lawson B, Wolthuis JS, Macdonald PD, Shepard CW, Williams IT, Armstrong GL, Gabel JA, Erwin P, Sheeler L, Kuhnert W, Patel P, Vaughan G, Weltman A, Craig AS, Bell BP, Fiore A. 2005. Molecular epidemiology of foodborne hepatitis A outbreaks in the United States, 2003. Journal of Infectious Diseases 192(30):1323–1330.
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